The laryngeal motor cortex: its organization and connectivity

Abstract

Our ability to learn and control the motor aspects of complex laryngeal behaviors, such as speech and song, is modulated by the laryngeal motor cortex (LMC), which is situated in the area 4 of the primary motor cortex and establishes both direct and indirect connections with laryngeal motoneurons. In contrast, the LMC in monkeys is located in the area 6 of the premotor cortex, projects only indirectly to laryngeal motoneurons and its destruction has essentially no effect on production of species-specific calls. These differences in cytoarchitectonic location and connectivity may be a result of hominid evolution that led to the LMC shift from the phylogenetically 'old' to 'new' motor cortex in order to fulfill its paramount function, that is, voluntary motor control of human speech and song production.

Figure 1

(A) The “Motor sequence” within the primary motor cortex with the extensive vocalization region in the inferior portion of the precentral gyrus [62]. (B) Meta-analysis of 19 fMRI studies between 2000-2013 using activation likelihood estimation (ALE) of brain function during voice production (GingerALE software). Bilateral peaks of LMC activation were found in the area 4p with an additional peak of activation in the left area 6 [15]. Data are presented on a series of sagittal slices in the standard Talairach-Tournoux space.

Figure 2

(A) Schematic drawing of the human brain and larynx (left) with the insets showing (top) the sites of vocalization elicitation during direct electrical stimulation of the primary motor cortex [63] and (bottom) the sagittal section of the brainstem depicting the distribution of degenerating fibers (small dots) in the nucleus ambiguus (Amb) and surrounding reticular formation [38]. The arrows represent the direct (monosynaptic) connections from the LMC to the reticular formation and nucleus ambiguus, the site of laryngeal motoneurons, which project to the laryngeal muscles (B) Schematic drawing of the macaque brain and larynx (left) with the insets illustrating (top) topographic representation of the intrinsic and extrinsic laryngeal muscle in the premotor cortex [4]. Sca –subcentral dimple; right-angled triangle – cricothyroid muscle; circle – thyroarytenoid muscle; encircled right-angled triangle - combination of the cricothyroid and thyroarytenoid muscles; square – extrinsic laryngeal muscles. (bottom) The crosssection of the brainstem and photomicrographs show terminal fields of the laryngeal motor cortical projections in the reticular formation (RF) but not nucleus ambiguus in the rhesus monkey, which was injected with the anterograde tracer, biotin dextranamine, into the LMC [36]. The arrows show indirect connection of the LMC with the nucleus ambiguus via the surrounding reticular formation. The scale bar corresponds to 50 μm.